Biologia 66/2: 335—339, 2011 Section Zoology DOI: 10.2478/s11756-011-0011-8
Mesostigmatic mites (Acari: Mesostigmata) in nests of the Eurasian griffon vulture (Gyps fulvus) in Croatia Jerzy Bloszyk1,2, Tvrtko Dražina3, Dariusz J. Gwiazdowicz4, Bruce Halliday5, Bartlomiej Goldyn1, Agnieszka Napierala1 & Eliza Rybska6 1
Department of General Zoology, Adam Mickiewicz University, Umultowska 89, 61-614 Pozna´ n, Poland; e-mail:
[email protected] 2 Natural History Collections, Faculty of Biology, Adam Mickiewicz University, Umultowska 89, 61-614 Pozna´ n, Poland; e-mail:
[email protected] 3 Department of Biology, Faculty of Science, University of Zagreb, Rooseveltov trg 6, Zagreb, 10000, Croatia; e-mail:
[email protected] 4 Department of Forest and Environment Protection, August Cieszkowski Agricultural University, Wojska Polskiego 71C, 60-625 Pozna´ n, Poland; e-mail:
[email protected] 5 CSIRO Ecosystem Science, GPO Box 1700, Canberra ACT 2601, Australia; e-mail:
[email protected] 6 The Faculty Laboratory of Nature and Biology Education, Adam Mickiewicz University, Umultowska 89, 61-614 Pozna´ n, Poland; e-mail:
[email protected]
Abstract: We examined the species composition and community structure of mites of the order Mesostigmata (Acari) in nests of the Eurasian griffon vulture (Gyps fulvus Hablizl, 1783) in Croatia. Material collected from 18 nests included 565 mites belonging to seven species. The most abundant species were Leiodinychus orbicularis (C.L. Koch, 1839) (Trematuridae) and Androlaelaps casalis (Berlese, 1887) (Laelapidae). The results were compared with the community structure and frequency of dominant species of Mesostigmata in nests of 32 other bird species. Leiodinychus orbicularis occurred in the nests of 13 species of birds. It is a typical nidicolous species which occurs most frequently in the perennial nests of birds of prey. In contrast, A. casalis rarely occurs in the nests of birds of prey. Key words: birds of prey; perennial nests; Acari; Uropodina; Gamasina; community structure
Introduction Bird nests are an example of unstable and isolated microhabitats that support a specific associated fauna, including various groups of invertebrates. The most abundant component of this associated fauna are arthropods, especially mites. Many birds build nests that last only for a single season, but the large perennial nests made by birds of prey and other birds such as storks allow the development of mite communities of definite structure and species composition (Philips 1981; Gwiazdowicz 2003a, b; Gwiazdowicz et al. 1999, 2000, 2005, 2006; Bajerlein et al. 2006; Bloszyk et al. 2005, 2006, 2009; Krištofik et al. 2009). The nests of birds provide opportunities to study the formation of animal communities that inhabit this microhabitat, and to follow the relationships between the bird hosts and the arthropods that occur in the nests. In many cases these relationships have a long history and a co-evolutionary character. The Eurasian griffon vulture (Gyps fulvus Hablizl, 1783) is a western Palaearctic species that occurs from India to Portugal. It breeds colonially on cliff ledges overlooking the sea, in large nests made of sticks and c 2011 Institute of Zoology, Slovak Academy of Sciences
grass. The insect fauna of these nests has been already surveyed (Dražina & Špoljar 2009) but the mite fauna is unknown, even though these nests appear to be a very attractive microhabitat for mites. These nests are characterised by considerable isolation and dispersion. Microhabitat conditions in these nests undergo cyclical changes depending on the biology of the host. The presence of birds in the nest changes and stabilises its microclimate, particularly during the incubating period, producing optimal conditions for the breeding of mites. At this time the nest contains food remains, excrement, and fragments of skin and feathers, which together provide a rich food supply for saprophagous invertebrates such as nematodes or insect larvae (Dražina & Špoljar 2009). These can occur in very large numbers in nests, and provide a potential food supply for predatory mites. Some parasitic species of mites that occur in nests are vectors that transmit virus and bacterial diseases to their bird hosts. Others may be beneficial to the birds, if they are predators that reduce the total parasite load. Studies of the composition and community structure of the commensal fauna in nests of birds thus provide an opportunity to broaden the knowledge of the biology and ecology of the host birds. This may be especially
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Table 1. List of mite species and number of specimens examined. Species
N
F
M
D
P
L
Leiodinychus orbicularis (C.L. Koch, 1839) Androlaelaps casalis (Berlese, 1887) Macrocheles ancyleus Krauss, 1970 Parasitus fimetorum (Berlese, 1904) Ameroseius macrochelae Westerboer, 1963 Poecilochirus austroasiaticus Vitzthum, 1930 Halolaelaps sp.
440 118 3 1 1 1 1
175 99 3 – 1 – –
157 13 – 1 – 1 –
80 6 – – – – 1
28 – – – – – –
– – – – – – –
Total
565
278
172
87
28
–
Explanations: N – total; F – females; M – males; D – deutonymphs; P – protonymphs; L – larvae.
Table 2. Abundance of mites from nests of the Eurasian griffon vulture. Colony Leiodinychus orbicularis Colony Cres Kruna Colony Cres Podokladi Colony Plavnik Androlaelaps casalis Colony Cres Kruna Colony Cres Podokladi Colony Plavnik
Nn
N
mean
±SD
F%
Range
8 6 4
117 58 265
16.7 14.5 88.3
21.4 15.9 88.1
87.50 66.67 75.00
1–62 2–36 35–190
8 6 4
79 7 32
15.8 2.3 10.7
16.7 1.5 8.1
62.5 50.0 75.0
2–42 1–4 5–20
Explanations: Nn – number of nests examined; N – number of specimens; mean – mean number of specimens per nest; ± SD – standard deviation; F% – frequency of occurrence in nests; range – minimum to maximum number of specimens per nest.
true when we compare the mite faunas of nests made by different species of birds that differ in their biology and breeding behaviour. The main aim of this study was to examine the species composition of Mesostigmata in nests of the griffon vulture, to determine which mite species are most abundant, most frequent, and most characteristic of this type of microhabitat. We also compare the mite communities of particular nests, to determine whether they have a similar structure, or whether they include an accidental combination of species. Further, we compare the mite fauna from nests of the Eurasian griffon vulture with those of nests made by other species of birds. Material and methods We collected material from 18 nests from three colonies of the Eurasian griffon vulture on the islands of Cres (two colonies) and Plavnik (one colony) in Croatia, in May 2004 and 2005. Each sample consisted of 1.5–2 L of nest material. A detailed description of the study area and the methods of collection was provided by Dražina & Špoljar (2009). The specimens are deposited in the Invertebrate Fauna Bank in the Faculty of Biology, Adam Mickiewicz University, Pozna´ n (AMU). The ecological analysis was based on calculation of Frequency (F%) and Dominance (D%) indices. The frequency and dominancy classes were determined according to Bloszyk (1999). The number of nests sampled was small, so a rigorous statistical analysis was not possible. The results should be regarded as preliminary observations only. SEM photographs were made in the Electron and Confocal Microscope Laboratory in the Faculty of Biology, AMU.
Results and discussion Community structure and sex ratio The mite community in the studied nests included seven species of Mesostigmata, and was heavily dominated by two of them. The material included 440 specimens of Leiodinychus orbicularis (C.L. Koch, 1839) (Trematuridae, also referred to as Trichouropoda orbicularis) and 118 of Androlaelaps casalis (Berlese, 1887) (Laelapidae). The other species were much less common, and were represented by very low numbers of individuals (Table 1). Leiodinychus orbicularis was more abundant than A. casalis in all colonies examined, but the relative abundance of the two species differed between colonies (Table 2). The largest number of mites was observed in nests from the colony located on the small island of Plavnik (Table 2), which yielded almost 100 mites per sample. This is the only colony sampled that has a south and southwest exposure; the other two are exposed to the east and northeast. This may produce higher temperatures in nests in the Plavnik colony, and favour the development of a more abundant nest fauna. Also, as a result of the prevailing wind in this area, this is the only colony situated on the leeward side of the island, which could also significantly affect the nest microclimate. The high abundance of L. orbicularis in nests in the Plavnik colony is not caused by a high abundance of insects in those nests, because these nests did not contain any of the insects that are used by mites for dispersal by phoresy (Histeridae, Staphylinidae, Trogidae, Scarabaeidae, Curculionidae, Tenebrionidae) (see Dražina & Špoljar 2009).
Mesostigmatic mites in nests of the Eurasian griffon vulture
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Fig. 1. Leiodinychus orbicularis. A – female, dorsal idiosoma; B – female, ventral idiosoma; C – male, ventral idiosoma; D – deutonymph, posterior tip of opisthosoma with attached pedicel.
Nests in both colonies on the larger island of Cres were characterised by a lower average number of mites, and the abundance of L. orbicularis was similar in all of them. The colony Crez Kruna had the highest number of mite species (six) and the highest average abundance
of A. casalis. In the Podokladi colony only three species were found, and nests here also had the lowest average number of mites per nest. The population structure of L. orbicularis shows that the dominant stage were adults (Figs 1A–C), with
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Table 3. Occurrence of Leiodinychus orbicularis in Uropodina communities in nests of selected bird species. Bird species Gyps fulvus (Hablizl, 1783) (griffon vulture) Ciconia ciconia (L., 1758) (white stork) Ciconia nigra (L., 1758) (black stork) Haliaeetus albicilla (L., 1758) (white-tailed eagle) Circus aeruginosus (L., 1758) (western marsh-harrier) Milvus milvus (L., 1758) (red kite) Ficedula hypoleuca (Pallas, 1764) (pied flycatcher) Sitta europaea L., 1758 (Eurasian nuthatch) Parus major L., 1758 (great tit) Cyanistes caeruleus (L., 1758) (blue tit) Sturnus vulgaris L., 1758 (European starling) Turdus merula L., 1758 (common blackbird) Phoenicurus phoenicurus (L., 1758) (common redstart) Passer montanus (L., 1758) (Eurasian tree sparrow)
Nn
U
F
D
18 38 31 35 2 2 79 3 78 15 36 43 2 9
1 11 10 8 1 3 1 2 1 2 2 9 1 2
C5 C5 C1 C1 C5 C4 C3 C5 C2 C4 C4 C1 C4 C5
D5 D5 D3 D1 D5 D1 D5 D5 D5 D5 D5 D3 D5 D5
Explanations: Nn – number of nests examined; U – number of Uropodina species in nests; F – frequency of occurrence of L. orbicularis: C1 – accidental, C2 – accessory, C3 – subconstant, C4 – constant, C5 – euconstant; D – degree of dominance of L. orbicularis: D1 – subrecedent, D2 – recedent, D3 – subdominant, D4 – dominant, D5 – eudominant (following Bloszyk 1999).
a sex ratio very close to 1 : 1 (Table 1) The absence of larvae and the low frequency of protonymphs indicates that the peak number of early juvenile stages does not occur during the May sampling period. Newly arrived phoretic deutonymphs (with pedicels, Fig. 1D) were observed only in the most north-facing colony on the island of Cres. These phoretic deutonymphs constituted up to 25% of all deutonymphs found in nests in the colony. This colony is situated closest to the mainland, and during the strong north to northeast bora winds it is on the windward side of the island, which may be conducive to delivering phoretic mites on insects from the mainland or the nearby island of Krk. Androlaelaps casalis females were much more common than males (M : F = 1 : 10). Populations of this species included no larvae or protonymphs. Comparison with other species of birds We examined data on the mites collected from more than 500 nests belonging to 32 species of birds, to establish which species support populations of L. orbicularis (data from “Invertebrate Fauna Bank”, computer database, AMU, Pozna´ n). We found records of L. orbicularis in the nests of 13 species of birds in addition to the griffon vulture (Table 3). The number of species of Uropodina in these nests varied from one to eleven. The frequency of L. orbicularis in nests of particular bird species was very variable, ranging from accidental occurrence (C1) to euconstant (C5). Its level of dominance was also very variable, from subrecedent (D1) to eudominant (D5). In nests of five species of birds, L. orbicularis was the only mite species observed – the griffon vulture, western marsh-harrier Circus aeruginosus (L., 1758), pied flycatcher Ficedula hypoleuca (Pallas, 1764), great tit Parus major L., 1758 and the common redstart Phoenicurus phoenicurus (L., 1758). Leiodinychus orbicularis is very frequent and abundant in nests of the white stork Ciconia ciconia (L., 1758), and much less frequent and abundant in those of the black stork Ciconia nigra (L., 1758) (Bloszyk & Gwiazdowicz 2006). It occurs most rarely in the nests of black
stork, white-tailed eagle Haliaeetus albicilla (L., 1758) and common blackbird Turdus merula L., 1758. Leiodinychus orbicularis is also known from soil and litter, but in those habitats it occurs rarely and at low densities. Bird nests seem to be the main habitat for this species. Its known range includes Europe and northern Africa (see Fig. 118 in Bloszyk 1999), but other literature records, for example in India, require verification. The second most abundant species of mite in these collections, A. casalis, has previously been found in nests of birds of prey as well as storks. It has also often been found in nest boxes of Passeriformes (Gwiazdowicz – personal observations). It has sometimes been regarded as parasitic, but there is evidence to show that it is actually a predator that can feed on parasites of birds (Lesna et al. 2009). The griffon vulture is attacked by a typical fauna of ectoparasites, including ticks (EstradaPe´ na et al. 1987), lice (Martin Mateo 1979), and feather mites (Dubinin 1956). It is possible that A. casalis is beneficial to the bird, by helping to suppress populations of these parasites in the nest. The other species of mites found in this study are much less abundant. Macrocheles ancyleus has often been found in perennial nests of birds of prey (Gwiazdowicz et al. 1999, 2000, 2005, 2006) and the black stork (Bloszyk et al. 2009), and it was also present in nests of the white stork (Bloszyk et al. 2005; Bajerlein et al. 2006; Bloszyk & Gwiazdowicz 2006), but only three specimens were found in this study. On the other hand, Poecilochirus austroasiaticus is typically associated with carrion (Korn 1983), and is carried phoretically by necrophilous beetles of the genus Nicrophorus. Parasitus fimetorum, represented by a single specimen, is often observed in nests of other birds and small mammals, and is also found in litter, compost, and similar habitats (Hyatt 1980). The remaining species, Ameroseius macrochelae and Halolaelaps sp., were also represented by one specimen each, and are considered as accidental occurrences in the studied nests.
Mesostigmatic mites in nests of the Eurasian griffon vulture Conclusions The mite fauna of nests of the griffon vulture is dominated by two species belonging to two different suborders of Mesostigmata. The only species from suborder Uropodina occurring in vulture nests is Leiodinychus orbicularis. Analysis of available data showed that this is a typical nidicolous species that occurs regularly in birds’ nests. It clearly prefers the long-term nests build by birds of prey, and it rarely occurs in passerine birds’ nests. Probably the major route of invading new nests is for this species is phoresy on insects. This is indicated by pedicels which were often found attached to deutonymphs in one of the populations. Most of the perennial nests made by birds of prey and storks in central Europe have much richer mite communities than those reported here. This is confirmed by observations of soil species, where communities in southern Europe, particularly in the Balkans, are qualitatively poorer (Bloszyk 1999). The number of Gamasina species found in vulture nests is also much lower than in perennial nests of such species as the white-tailed eagle, white stork and black stork. However, due to the fact that only few nests were examined in the present study, these observations should be regarded as preliminary, and statistical confirmation of the results requires further studies based on more extensive sampling. Acknowledgements The authors thank Dr. Z. Adamski from the Laboratory of Electron and Confocal Microscopy. This paper is a result of Research Project No. 2/216/WI/09. Special thanks go to Dr. G. Su´ ni´c, who enabled collecting this material during the ringing activities of G. fulvus in 2004 and 2005. References Bajerlein D., Bloszyk J., Gwiazdowicz D.J., Ptaszyk J. & Halliday B. 2006. Community structure and dispersal of mites (Acari, Mesostigmata) in nests of the white stork (Ciconia ciconia). Biologia 61: 525–530. DOI: 10.2478/s11756-006-00869 Bloszyk J. 1999. Geograficzne i ekologiczne zró˙znicowanie roztoczy z kohorty Uropodina (Acari: Mesostigmata) w Polsce. I. Uropodina lasów gr˛adowych (Carpinion betuli). Kontekst, Pozna´ n, 245 pp. Bloszyk J. & Gwiazdowicz D.J. 2006. Acarofauna of nests of the White Stork Ciconia ciconia, with special attention to mesostigmatid mites, pp. 407–414. In: Tryjanowski P., Sparks T.H. & Jerzak L. (eds), The White Stork in Poland: Studies in Biology, Ecology and Conservation, Bogucki Wydawnictwo Naukowe, Pozna´ n.
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